Interplay between cytoplasmic Ca2+ and the ATP/ADP ratio: a feedback control mechanism in mouse pancreatic islets

Biochem J. 1998 Jul 15;333 ( Pt 2)(Pt 2):269-74. doi: 10.1042/bj3330269.

Abstract

In pancreatic beta cells, the increase in the ATP/ADP ratio that follows a stimulation by glucose is thought to play an important role in the Ca2+-dependent increase in insulin secretion. Here we have investigated the possible interactions between Ca2+ and adenine nucleotides in mouse islets. Measurements of both parameters in the same single islet showed that the rise in the ATP/ADP ratio precedes any rise in the cytoplasmic free-Ca2+ concentration ([Ca2+]i) and is already present during the initial transient lowering of [Ca2+]i produced by the sugar. Blockade of Ca2+ influx with nimodipine did not prevent the concentration-dependent increase in the ATP/ADP ratio produced by glucose and even augmented the ratio at all glucose concentrations which normally stimulate Ca2+ influx. In contrast, stimulation of Ca2+ influx by 30 mM K+ or 100 microM tolbutamide lowered the ATP/ADP ratio. This lowering was of rapid onset and reversibility, sustained and prevented by nimodipine or omission of extracellular Ca2+. It was, however, not attenuated after blockade of secretion by activation of alpha2-adrenoceptors. The difference in islet ATP/ADP ratio during blockade and stimulation of Ca2+ influx was similar to that observed between threshold and submaximal glucose concentrations. The results suggest that the following feedback loop could control the oscillations of membrane potential and [Ca2+]i in beta cells. Glucose metabolism increases the ATP/ADP ratio in a Ca2+-independent manner, which leads to closure of ATP-sensitive K+ channels, depolarization and stimulation of Ca2+ influx. The resulting increase in [Ca2+]i causes a larger consumption than production of ATP, which induces reopening of ATP-sensitive K+ channels and arrest of Ca2+ influx. Upon lowering of [Ca2+]i the ATP/ADP ratio increases again and a new cycle may start.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adenosine Diphosphate / metabolism*
  • Adenosine Triphosphate / metabolism*
  • Animals
  • Calcium / metabolism*
  • Calcium Channel Blockers / pharmacology
  • Cytoplasm / metabolism*
  • Female
  • Glucose / metabolism
  • Hypoglycemic Agents / pharmacology
  • Insulin / metabolism
  • Islets of Langerhans / metabolism*
  • Mice
  • Nimodipine / pharmacology
  • Potassium / metabolism
  • Tolbutamide / pharmacology

Substances

  • Calcium Channel Blockers
  • Hypoglycemic Agents
  • Insulin
  • Nimodipine
  • Adenosine Diphosphate
  • Adenosine Triphosphate
  • Tolbutamide
  • Glucose
  • Potassium
  • Calcium